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Mechanisms of Niche Adaption by Yersinia

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Mechanisms of Niche Adaption by Yersinia University of Veterinary Medicine Hannover Mechanisms of niche adaption by Yersinia THESIS submitted in partial fulfillment of the requirements for the degree of Doctor rerum naturalium (Dr. rer. nat) awarded by the University of Veterinary Medicine Hannover by Carina Maria Schmühl 08.02.1990, Düren Hannover, Germany 2018 Supervisor: Prof. Dr. Petra Dersch Supervision Group: Prof. Dr. Petra Dersch (Helmholtz Centre for Infection Research, Braunschweig) Prof. Dr. Peter Valentin-Weigand (University of Veterinary Medicine Hannover) PD Dr. Simone Bergmann (Technical University Braunschweig) 1st Evaluation: Prof. Dr. Petra Dersch (Department of Molecular Infection Biology, Helmholtz Centre for Infection Research, Braunschweig) Prof. Dr. Peter Valentin-Weigand (Institute for Microbiology, University of Veterinary Medicine Hannover) PD Dr. Simone Bergmann (Institute of Microbiology, Technical University Braunschweig) 2nd Evaluation: Prof. Dr. Thilo Fuchs (Institute of Molecular Pathogenesis, Friedrich- Loeffler-Institut, Jena) This PhD Thesis was performed at the Helmholtz Centre for Infection Research, Braunschweig, at the Department of Molecular Infection Biology. Date of final exam: 30.10.2018 Sponsorship: Carina Maria Schmühl was supported within the Ph.D. program ’Animal and Zoonotic Infections’ by a Lichtenberg Fellowship from the Niedersächsische Ministerium für Wissenschaft und Kultur (MWK). Parts of this thesis have been published previously: Publications Nuss A, Beckstette M, Pimenova M, Schmühl C, Opitz W, Pisano F, Heroven AK, Dersch P. 2017. Tissue dual RNA-seq allows fast discovery of infection-specific functions and riboregulators shaping host-pathogen transcriptomes. Proc Natl Acad Sci USA. 114(5): E791-E800. doi: 10.1073/pnas.1613405114. Schmühl C, Beckstette M, Heroven AK, Bunk B, Spröer C, McNally A, Overmann J, Dersch P. 2018. Comparative transcriptomic profiling of Yersinia enterocolitica O:3 and O:8 reveals major expression differences of fitness- and virulence-relevant genes indicating ecological separation. Nucleic Acid Res. Submitted. Conference participations Nuss AM, Beckstette M, Schmühl C, Pisano F, Heroven AK, Reinkensmeier J, Dersch P.: Tissue Dual RNA-seq of Yersinia pseudotuberculosis and murine Peyers Patches. (Poster Presentation) 5th National Yersinia Meeting. Münster, 2016. Schmühl C, Nuss A, Heroven AK, Beckstette M, Dersch P.: Mechanisms of the adaption and persistence of Yersinia enterocolitica. (Poster Presentation) Microbiology and Infection 2017 - 5th Joint Conference of the DGHM & VAAM. Würzburg, 2017. Schmühl C, Beckstette M, Heroven AK, Nuss A, Dersch P.: Transcriptional landscape of Yersinia enterocolitica O:8 and O:3. (Poster Presentation) Annual Conference of the Association for General and Applied Microbiology (VAAM). Wolfsburg, 2018. Schmühl C, Beckstette M, Heroven AK, Nuss A, Dersch P.: Transcriptional landscape of Yersinia enterocolitica O:8 and O:3. (Oral presentation) European Yersinia Conference. Jena, 2018. Schmühl C, Beckstette M, Heroven AK, Nuss A, Dersch P.: Transcriptional landscape of Yersinia enterocolitica O:8 and O:3. (Poster Presentation) Young Microbiologist Symposium on Microbe Signaling, Organization and Pathogenesis. Belfast, 2018. Table of Contents Table of Contents TABLE OF CONTENTS I LIST OF ABBREVIATIONS I LIST OF FIGURES I LIST OF TABLES I 1 SUMMARY 1 1 ZUSAMMENFASSUNG 3 2 INTRODUCTION 5 2.1 THE GENUS YERSINIA 6 2.2 INFECTION ROUTE OF ENTEROPATHOGENIC YERSINIAE 8 2.3 SEROTYPES OF YERSINIA ENTEROCOLITICA 11 2.4 RESERVOIRS OF ENTEROPATHOGENIC YERSINIAE 14 2.5 VIRULENCE FACTORS OF ENTEROPATHOGENIC YERSINIAE 15 2.5.1 UREASE 15 2.5.2 MOTILITY 15 2.5.3 ADHESINS AND INVASINS 16 2.5.3.1 Invasin 16 2.5.3.2 Ail 18 2.5.3.3 YadA 18 2.5.4 THE PLASMID-ENCODED YSC TYPE-3-SECRETION SYSTEM 19 2.5.5 LIPOPOLYSACCHARIDES 20 2.6 Y. ENTEROCOLITICA STRAIN SPECIFIC VIRULENCE GENES 23 2.7 RNA-SEQUENCING AS A GLOBAL APPROACH TO IDENTIFY NEW REGULATORY RNAS 25 2.8 AIM OF THE STUDY 30 2.9 REFERENCES 31 3 PUBLICATION 1 47 4 PUBLICATION 2 49 4.1 ABSTRACT 50 4. 2 INTRODUCTION 50 4.3 MATERIAL AND METHODS 52 4.4 RESULTS AND DISCUSSION 59 4.4.1 COMPARATIVE RNA-SEQ OF Y. ENTEROCOLITICA O:8 AND O:3 59 4.4.2 GENOME-WIDE ANALYSIS OF TRANSCRIPTIONAL START SITES 62 4.4.3 GLOBAL ANALYSIS OF THE PROMOTER REGIONS AND ARCHITECTURE 63 4.4.4 THE REPERTOIRE OF Y. ENTEROCOLITICA NON-CODING RNAS 65 4.4.5 MONITORING OF INFECTION-RELEVANT CHANGES IN YEO:3 AND YEO:8 GENE EXPRESSION 67 4.4.6 DIFFERENTIAL EXPRESSION OF THE YSTA TOXIN GENE 76 4.5 CONCLUSIONS 79 4.6 DATA AVAILABILITY 81 4.7 SUPPLEMENTARY DATA 81 4.7.1 SUPPLEMENTARY TABLES 81 I Table of Contents 4.7.2. SUPPLEMENTARY FIGURES 86 4.8 ACKNOWLEDGEMENT 92 4.9 FUNDING 92 4.10 REFERENCES 92 5 DISCUSSION 99 5.1 GLOBAL MAPPING OF TRANSCRIPTIONAL START SITES IN YERSINIA 99 5.2 THE YERSINIA REPERTOIRE OF NON-CODING RNAS 102 5.3 CHANGES IN THE GENE EXPRESSION PROFILE 105 5.4 REFERENCES 114 6 OUTLOOK 121 7 APPENDIX 123 7.1 CURRICULUM VITAE 123 7.3 ACKNOWLEDGMENT 124 II List of Abbreviations List of Abbreviations °C degree Celsius asRNA antisense RNA BHI Brain-heart infusion bp base pairs CDS coding sequence cDNA complementary DANN cfu colony forming unit Csr Carbon storage regulator DC dendritic cell DNA deoxyribonucleic acid dsDNA double-stranded DNA et al. et alii FC fold change g gram GalNac N-acetyl-galactosamine h hour(s) kb kilobasepairs kDa Kilodalton l liter LPS lipopolysaccharide mM millimolar M molar M cell Microfold cell mg milligram ml mililiter MLN mesenteric lymph node mRNA messenger RNA ncRNA non-coding RNA nt nucleotides ORF open reading frame PCR polymerase chain reaction PMN polymorphonuclear cells neutrophil PP(s) Peyer’s patch(es) pYV plasmid of Yersinia virulence qRT-PCR quantitative real-time reverse transcription-PCR RNA ribonucleic acid RNA-seq RNA-sequencing RPKM reads per kilobase transcript length per million mapped reads rRNA ribosomal RNA sRNA small regulatory RNA T3SS Type-3-Secretion-System TCA tricarboxylic acid TEX Terminator-5’-Phosphate-Dependent-Exonuclease TSS transcriptional start site UTR untranslated region YeO:3 Yersinia enterocolitica serotype O:3 YeO:8 Yersinia enterocolitica serotype O:8 III List of figures List of figures Figure 2.1: The phylogeny of the genus Yersinia. ................................................................... 8 Figure 2.2: Invasion of enteropathogenic Yersinia into epithelial M-cells and underlying lymphatic tissues. ................................................................................................................... 10 Figure 2.3: Gene gain and gene loss in Y. enterocolitica. Y. enterocolitica strains are subdivided into different phylogoups. ..................................................................................... 12 Figure 2.4: Schematic overview of virulence factors of enteropathogenic Yersinia expressed on the cell surface. ................................................................................................................. 16 Figure 2.5: Schematic representation of the ysc T3SS. ......................................................... 20 Figure 2.6: Schematic representation of the Y. enterocolitica O:3 lipopolysaccharide. ......... 21 Figure 2.7: Temperature-dependent variations of lipid A in Y. enterocolitica. ........................ 23 Figure 2.8: Model of regulation mechanisms by regulatory RNAs. ........................................ 28 Figure 4.1: Comparative RNA-seq workflow and global reports. ........................................... 61 Figure 4.2: Comparative analysis of mRNA transcriptional start sites (TSSs) of Y1 and 8081v. .................................................................................................................................... 63 Figure 4.3: Identification of ncRNAs of YeO:3 Y1 and YeO:8 8081v. .................................... 65 Figure 4.4: Comparison of the growth- and temperature-dependent regulons of YeO:3 Y1 and YeO:8 8081v. .................................................................................................................. 66 Figure 4.5: Bacterial global gene expression analysis of YeO:3 Y1 and YeO:8 8081v uncovers strain-specific metabolic and stress adaptations.. .................................................. 71 Figure 4.6: Differentially regulated virulence functions between strains YeO:3 Y1 and YeO:8 8081v. .................................................................................................................................... 74 Figure 4.7: Analysis of ystA expression in Y. enterocolitica.. ................................................. 75 Figure 4.8: Influence of H-NS, YmoA and RovA on ystA expression of Y. enterocolitica strain Y1.. ......................................................................................................................................... 78 Figure S4.1: Average nucleotide identity of the YeO:3 strain Y1 with other Y. enterocolitica and Y. pseudotuberculosis strains. ........................................................................................ 86 Figure S4.2: Global identification of mRNA transcriptional start sites (TSSs). ....................... 87 Figure S4.3: Identification of ncRNAs of YeO:3 Y1 and YeO:8 8081v. .................................. 88 Figure S4.4: Comparison of gene expression changes obtained by RNA-seq and real-time qRT-PCR. ............................................................................................................................... 89 Figure S4.5: Gene expression
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